Download The effect of obligate hyperparasitoids on biological control: Differential

The effect of obligate hyperparasitoids on biological control: Differential
vulnerability of primary parasitoids to hyperparasitism can mitigate
trophic cascades
Robert S. Nofemela*
Insect Ecology Division, ARC-Plant Protection Research Institute, Private
Bag X134, Queenswood 0121, South Africa Department of Zoology &
Entomology, University of Pretoria, Private Bag X20, Pretoria 0028,
South Africa. *Email: [email protected]
Highlights
-Cotesia vestalis was a dominant primary parasitoid of Plutella xylostella.
-It was also a secondary host to three obligate hyperparasitoid species.
-At low hyperparasitism, C. vestalis limited hosts available to competitors.
-As C. vestalis population declined, competitors parasitized more of available hosts.
-Species that are invulnerable to hyperparasitism took over role of the vulnerable.
Graphical abstract
Abstract : Obligate hyperparasitoids are widely considered an important ecological disturbance
to biological control of insect pests, as they develop at the expense of primary parasitoids.
However, supporting evidence is largely derived from direct trophic interactions in simple food
webs. Yet, a multitude of insect pest populations simultaneously support development of several
primary parasitoid species in horticultural and natural systems. Since primary parasitoid species
in a community can differ in vulnerability to obligate hyperparasitoids, it is desirable to establish
if the invulnerable primary parasitoids can take advantage of reduced competition from affected
species by increasing their contribution to total primary parasitism levels thereby mitigating
effects of hyperparasitism on biological control. To investigate this question, populations of the
diamondback moth, Plutella xylostella (Linnaeus) (Plutellidae), its primary parasitoids and
hyperparasitoids were monitored on unsprayed cabbage plots at weekly intervals over six
consecutive years. Cotesia vestalis (Haliday) (Braconidae), a dominant primary parasitoid in this
system, was a secondary host to three obligate hyperparasitoids: Mesochorus sp.
(Ichneumonidae), Eurytoma sp. (Eurytomidae) and Pteromalus sp. (Pteromalidae). The higher
efficiency of C. vestalis in utilizing younger host larvae at lower hyperparasitism levels limited
host availability to other major primary parasitoids. But, as hyperparasitism levels increased and
its populations declined, populations of Oomyzus sokolowskii (Kurdjumov) (Eulophidae) and
Diadromus collaris (Gravenhorst) (Ichneumonidae) increased significantly as they parasitized a
greater proportion of available hosts. As a consequence, the impact of hyperparasitoids did not
result in trophic cascades, as their impact on total primary parasitism levels and infestation levels
was insignificant. This study shows that primary parasitoid species that are invulnerable to
hyper-parasitism can take over the function of vulnerable ones in communities where
interspecific interactions among species are strong. Thus, an approach that considers both direct
and indirect effects of hyperparasitoids in primary parasitoid communities improves our
understanding of the net impact of hyperparasitism on biological control of insect pests.
Keywords: Plutella xylostella Infestation level Primary parasitism Hyperparasitism Top-down
effect Developmental traits Functional diversity
1. Introduction
Biological control theory suggests that consumer species can effectively suppress their host or
prey populations (Hairston et al., 1960; Crawley, 1989). However, the strong top-down effect of
consumers not only influences the population size of prey/hosts, but can indirectly influence
population densities of species in lower trophic levels. This propagation of strong effects of
higher-order consumers through the food web is called a trophic cascade (Polis et al., 2000). In a
simple food web involving a host plant – an insect herbivore – a primary parasitoid, high
parasitism of the herbivore population benefits the host plant if infestation levels are reduced
(Murdoch and Briggs, 1996; Hawkins and Cornell, 1999; Matsumoto et al., 2003). Although
primary parasitoids are widely utilized for biological control of insect pests (DeBach and Rosen,
1991), they do not occupy the highest trophic level. Due to direct relevance of trophic cascades
to biological control practice, the effect of secondary parasitoids (hereafter referred to as
‘hyperparasitoids’) on efficiency of primary parasitoids is an important topic in biological
control (Rosen, 1981; Rosenheim, 1998; Sullivan and Völkl, 1999).
Four types of hyperparasitoids are described (Sullivan and Völkl, 1999; Walter and Abeeluck,
2006); but only two types (i.e., facultative and obligate) are found where Lepidoptera are plant
pests (Sullivan and Völkl, 1999), which is a focus of this study. Facultative hyperparasitism is a
form of omnivory, where a parasitoid feeds on two trophic levels by acting both as a primary
parasitoid and a hyperparasitoid (Brodeur, 2000). However, this group of hyperparasitoids is not
considered detrimental to biological control, except where they selectively parasitize primary
parasitoids more than the insect pest population (Moore and Kfir, 1995; Pérez-Lachaud et al.,
2004). In contrast, obligate hyperparasitoids only reproduce on primary parasitoids, and this
direct impact on primary parasitoid populations has made them the most studied hyperparasitoid
group (Clausen, 1972; Sullivan and Völkl, 1999). They are divided into two subcategories: (1)
those attacking larvae of primary parasitoids through the body of insect pests and, (2) those
attacking primary parasitoid pupae outside the body of insect pests (Sullivan and Völkl, 1999).
The presence of both subcategories in a food web can alter the food web structure if those
species attacking primary parasitoid pupae also parasitize species attacking larval stages (Carew
and Sullivan, 1993; Brodeur, 2000).
A majority of studies have shown that presence of obligate hyperparasitoids increases herbivory
as insect pest populations are often released from the strong top-down effect of primary
parasitoids (Bourchier and Nealis, 1992; Eichhorn, 1996; Boenisch et al., 1997; Lei and Hanski,
1997; Rosenheim, 1998; Brodeur, 2000; Schooler et al., 2011). Further, obligate
hyperparasitoids can leave cues on the plant surface that may increase dispersal probability of
primary parasitoids, which further reduces mortality of insect pests (Höller et al., 1993; van
Veen et al., 2001). However, other studies have shown that the impact of obligate hyperparasitoids is not always sufficiently large to result in trophic cascades (Cameron and Walker, 2002;
Roltsch et al., 2006; Araj et al., 2009) due to: (1) the ability of some primary parasitoids to
modify the behavior of parasitized hosts (Brodeur and McNeil, 1992; Tanaka and Ohsaki, 2006,
2009), (2) density-independent hyperparasitoid aggregation (Weseloh, 1986; Ayal and Green,
1993; Schooler et al., 1996; Müller and Godfray, 1998), and (3) lower reproductive potential of
obligate hyperparasitoids compared to their primary parasitoid hosts (Brodeur, 2000).
Although these studies provided important basic knowledge of differential impact of obligate
hyperparasitoids on biological control of insect pests, they largely investigated this indirect effect
using direct trophic interactions. Yet, a multitude of insect herbivore populations are known to
simultaneously support development of several primary parasitoid species in natural and
horticultural systems (Godfray, 1994; Hawkins, 1994; Müller et al., 1999). Although obligate
hyperparasitoids are not host-specific, they do not just attack any primary parasitoid species as
their host range is restricted by developmental traits of their hosts (Grasswitz and Reese, 1998;
Chow and Mackauer, 1999; Schwarz and Shaw, 2000; Day, 2002). Thus, primary parasitoid
species that perform the same function in a community (e.g., egg, larval or pupal parasitoids, and
thus are functionally redundant; Loreau, 2004; Casula et al., 2006) may be equally vulnerable to
obligate hyperparasitoids that require their shared traits (Clausen, 1972). However, primary
parasitoids that attack different life stages of a common host population (i.e., they perform
different functions in the community, and thus are functionally complementary; Wilson et al.,
1999; Cardinale et al., 2003; Veddeler et al., 2010) usually have different suites of
hyperparasitoids. Thus, the developmental traits of primary parasitoid species in a community
determine whether a given obligate hyperparasitoid produces species-level or community-level
trophic cascades (see Polis et al., 2000; Schmitz et al., 2000).
The life stages of the diamondback moth, Plutella xylostella (Linnaeus) (Lepidoptera:
Plutellidae), are attacked by several species of primary parasitoids in South Africa, of which
Cotesia vestalis (Haliday) [= Cotesia plutellae (Kurdjumov)], a solitary koinobiont larval
parasitoid, is the most dominant. However, its larval and pupal stages are in turn attacked by
three species of obligate hyperparasitoids (Waladde et al., 2001; Mosiane et al., 2003; Smith,
2004; Nofemela and Kfir, 2005). In this study, I use long-term data sets to establish whether: (1)
the effect of obligate hyperparasitoids on C. vestalis populations are significantly high to limit its
impact on P. xylostella, (2) the invulnerable primary parasitoid species increase their
contribution to total parasitism levels as populations of C. vestalis decline, and (3) the population
increase of invulnerable primary parasitoids effectively counteracts the effect of hyperparasitoids
on C. vestalis.
2. Materials and methods
2.1. Study area
The study reported here was conducted on a research farm belonging to the ARC-Institute for
Industrial Crops at Brits (25° 59' S, 27° 76' E, altitude 1 082 m), North West Province of South
Africa. The Brits municipality area is within the Highveld, i.e., a high plateau inland region
characterized by temperate climate and summer rainfall (Rutherford et al., 2006). The study site
is within the Marikana Thornveld, a component of the Savannah Biome, where dominant natural
vegetation is Acacia karroo. The soil type is mainly vertic melanic clays with some dystrophic or
mesotrophic plinthic catenas and some freely drained, deep soils. Long-term annual precipitation
is between 600 and 700 mm, and mean maximum and minimum temperatures are 35.3 °C and 3.3 °C for January and June, respectively (Rutherford et al., 2006). Several species of wild
Brassica species are abundant during rainy months in South Africa (Jordaan, 1993), and these
are known to be important reservoirs for P. xylostella and its parasitoids that later move into
cultivated crucifers (Ullyett, 1947; Kahuthia-Gathu et al., 2009). Cabbage [Brassica oleraceae
variety capitata (Linnaeus) (Brassicaceae)] is one of the major crops grown under irrigation in
farms within 5 km radius of the study site. Commercial growers transplant cabbage seedlings on
several hectares, usually 25,000 cabbages/ha, every week during summer and autumn, but few
hectares are planted during winter and summer months (Multi-plant nursery, Brits, personal
communication). It appears that the major reason for transplanting fewer cabbages during cool
seasons is influenced by slower developmental rate of the crop, which affects produce flow rate
from the farm. Since immature Brassica plants were always present at any given moment at a
landscape level around the study site, the cabbage fields are assumed to be connected [i.e.,
metapopulation theory] due to free movement of P. xylostella and its parasitoids between the
farms (Vandermeer and Carvajal, 2001; Desouhant et al., 2003; Gichini et al., 2008).
2.2.
Monitoring of P. xylostella infestations and its parasitoids
Cabbage seedlings (between 2000 and 2500) were transplanted three consecutive times per
year, from February 2002 to January 2008, at a plant spacing of 0.5 m within and 1 m between
rows. Standard agronomic practices that included plowing, irrigation, fertilization, and weeding
were followed in each crop, but without application of insecticides. For each crop, monitoring of
P. xylostella infestations (i.e., larvae and pupae) and its parasitoids was initiated two weeks after
cabbage transplants. In subsequent plantings, a new crop was prepared next to the old one five
weeks before harvest of the current crop, and two weeks later scouting on the older plot was
terminated and begun on the new plot. This practice ensured that investigations were continually
conducted on crops of reasonably good quality. Therefore, until it was completely harvested and
remaining plants plowed under, the older crop served as a reservoir for P. xylostella and its
parasitoids at a local scale. One experimental plot was monitored at any given time and a total of
18 plots were monitored during the study period.
At weekly intervals, leaves of 30 randomly selected plants in each crop were thoroughly
inspected and numbers of P. xylostella larvae, pupae, and its parasitoid pupae found in each plant
were recorded. Since no egg parasitoid species have been recorded from P. xylostella in South
Africa (Kfir, 1997), parasitism levels were determined from samples of host larvae and pupae,
and pupae of its parasitoids. However, 1st and 2nd instar larvae were not sampled for all known
P. xylostella egg-larval and larval parasitoids complete their larval development once the hosts
have reached the fourth instar. Thus, parasitism of P. xylostella eggs and larvae accumulates over
the larval instars (Nofemela and Kfir, 2005, 2008). Further, sampling of host instars that are still
vulnerable to parasitism is inappropriate, as it tends to grossly underestimate parasitism levels
(van Driesche et al., 1991). Depending on the number of cabbages that were transplanted and
season, the number of sampled plants during summer and autumn accounted for 14.4-18% of
plant population, and 19.2-24% of plant population during winter and spring. Thus, sampling
hardly influenced population densities of the pest and its parasitoids.
2.3.
The determination of primary parasitism and hyperparasitism
levels of P. xylostella
The field-collected samples were maintained in the insectary of the ARC-Plant Protection
Research, Rietondale campus (25° 44' S, 18° 13' E), in Pretoria, at 25 ± 1 °C, 65 ± 5% rh., and
L16: D8 photo-period. The larvae were provided with sections of fresh cabbage leaves and held
individually in Petri dishes. The leaves were replaced every second day until all the larvae
pupated or parasitoid pupae formed. The samples of P. xylostella pupae and parasitoid pupae
were confined individually in ventilated glass vials (2.5 x 10 cm). All emergent parasitoids were
identified and their incidence determined. Voucher specimens were deposited in the National
Collection of Insects, Biosystematics Division, ARC-Plant Protection Research Institute,
Pretoria. Parasitism (primary and hyperparasitism) was calculated as the percentage of emergent
parasitoids out of total samples of P. xylostella larvae and pupae, and parasitoid pupae. Thus, the
impact of primary parasitoids on P. xylostella population density was determined from parasitism of corresponding infestation levels. However, samples that died of unknown causes were
excluded from calculations of parasitism.
2.4. Data analysis
One-way analysis of variance (ANOVA) was used to compare the incidence of the different
primary parasitoid and hyperparasitoid species. Where significant differences were detected
between incidences of the parasitoids, the means were compared using Fisher’s protected least
significance (LSD) test. Using mean values obtained over 6 years for each corresponding week
(i.e., from week 1 in February to week 52 in January), linear regression analyses were performed
to determine the influence of hyperparasitism on C. vestalis population densities over the course
of the year, and the responses of unaffected primary parasitoid species populations as
hyperparasitism levels increase. For all statistical analyses, the level of significance was set at
5% and the analyses were performed using Statistica (2012).
3. Results
Out of the 4476 samples of P. xylostella larvae and pupae, and pupae of primary parasitoids
[i.e., the larval parasitoids C. vestalis and Apanteles halfordi (Ullyett) (Braconidae), and the
larval-pupal parasitoid Diadegma mollipla (Holmgren) (Ichneumonidae)] collected during this
study, a total of four primary parasitoid species and a facultative hyperparasitoid (Fig. 1) and
three species of obligate hyperparasitoids (Fig. 2) were recorded.
The incidence of the primary parasitoid species differed greatly (F4,1128 = 235.73; P< 0.001)
on P. xylostella population with C. ves-talis dominating the primary parasitoid community
followed by the facultative hyperparasitoid Oomyzus sokolowskii (Kurdjumov) (Eulophidae), a
larval-pupal parasitoid (Fig. 1). This result is in agreement with previous studies on biological
control of P. xylostella in South Africa (Kfir, 1997; Waladde et al., 2001; Mosiane et al., 2003;
Smith, 2004; Nofemela and Kfir, 2005, 2008).
Although 0. sokolowskii may attack C. vestalis larvae inside the primary host (Mahmood et al.,
2003; Shi and Liu, 2003), it is considered more of a primary parasitoid than a hyperparasitoid in
South Africa (Nofemela and Kfir, 2008), and in few other countries (Jamaica: Alam, 1992; Cape
Verde: Cock, 1983). This view is upheld in this study for it attacked significantly (t = 43206; d.f.
= 443; P< 0.001) more P. xylostella (mean ± SD = 8.0574 ± 15.9473) than C. vestalis (2.2841 ±
11.2639). The realized clutch size of 0. sokolowskii was significantly higher (t= 5.3186; df. =
184; P< 0.001) from P. xylostella pupae (9.0693 ± 3.399) than from C. vestalis pupae (4.0 ±
1.6833). The primary host density influences levels of hyper-parasitism by facultative
hyperparasitoids, and consequently their impact on primary parasitoid populations in some
systems (Borer et al., 2003), but hyperparasitic activity of 0. sokolowskii was independent (r2 =
0.0144; F1, 50 = 0.7296; P = 0.3971; y = 10. 6127 -0.0451) of P. xylostella infestations in this
study.
The impact of 0. sokolowskii on C. vestalis populations was similar to that of obligate
hyperparasitoids: Mesochorus sp. (Ichneumonidae) (3.1263 ±0.66) and Pteromalus sp.
(Pteromalidae) (2.3345 ± 0.7497) whose incidence was significantly higher (F3, 707 = 3.116; P =
0256; Fig. 2) than Eurytoma sp. (Eurytomidae) (0.1503 ± 0.7497). Mesochorus sp. attacks C.
vestalis larvae through the body of P. xylostella aided by its long ovipositor, and its offspring
completes pupal development inside pupae of C. vestalis (Clausen, 1972; Kfir, 1997).
Pteromalus sp. and Eurytoma sp. directly attack pupae of C. vestalis (Nofemela and Kfir, 2005).
The obligate hyperparasitoids were active for most of the year, except during winter months
(June-August), albeit generally at low levels individually (Fig. 2), but their combined
average
impact (which includes 0. sokolowskii) on C. vestalis populations was significant (r2 = 0.1151;
F1, 50 = 6.5016; P< 0.0139; y = 67.4624-0.7676x; Fig. 3) during periods of high activity. Since P.
xylostella egg and egg-larval parasitoids are rare in South Africa (Kfir, 1997), the higher
efficiency of C. vestalis in utilizing young host larvae (Nofemela, 2004) can limit availability of
healthy hosts for primary parasitoids attacking older larvae and advanced life stages. The
primary parasitoids that took advantage of decreasing C. vestalis population density 2 by
increasing their populations, as hyperparasitism levels increased were 0. sokolowskii (r =
0.2513; F1, 50 = 16.7817; P< 0.001; y = 5.9518
+ 0.5113x) and Diadromus collaris
(Gravenhorst) (Ichneumonidae), a pupal parasitoid, (r2 = 0.1592;2 F1, 47 = 8.8959; P = 0.0045; y =
1.3172 + 0.167x). Thus, a significantly negative relationship (r = 0.3517; F1, 50 = 27.1276; P<
0.001; y = 41.0434-0.3639x) between incidence of C. vestalis and the two major primary
parasitoids was observed.
While performance of 0. sokolowskii and D. collaris was clearly impeded by the high
efficiency of C. vestalis at low hyperparasitism levels, but D.2 mollipla (r2 = 0.0000; F1, 50 =
0.0001; P= 0.9921; y = 0.1955 + 0.0001x) and A halfordi (r = 0.0022; F1, 50 = 0.1081; P =
0.7437; y = 0.8842 + 0.0109x) populations remained low even when competition with C. vestalis
was reduced by hyperparasitism. In fact, D. mollipla was recorded in just 6 occasions and A
halfordi in 25 out of the total of 254 scouting events where P. xylostella larvae were recorded.
The increases in populations of 0. sokolowskii and D. collaris were sufficiently large to
counteract the impact of hyperparasitoids on C. vestalis
populations, as hyperparasitism did not
negatively influence total primary parasitism levels (r 2 = 0.0427; F1, 50 = 2.2313; P = 0.1415; y
= 49.8155 + 0.6193x) nor led to higher P. xylostella infestations (^ = 0.0207; F1, 50 = 1.0585; P =
0.3085; y = 0.9209 + 0.0285x).
4. Discussion
The indirect influence of obligate hyperparasitoids on biological control of insect pests through
direct impact on populations of primary parasitoids has grasped attention of biological control
practitioners for decades (Rosen, 1981; Rosenheim, 1998; Sullivan and Völkl, 1999; Brodeur,
2000). Since the majority of studies showed that hyperparasitoids release insect pest populations
from the strong top-down effect of primary parasitoids, it is generally recommended that
introduction of hyperparasitoids should be avoided (Sullivan and Völkl, 1999). Although it is
possible to exclude them during quarantine assessments of primary parasitoid consignments,
primary parasitoids can acquire other obligate hyperparasitoid species once released in the field
(Agricola and Fisher, 1991; Bourchier and Nealis, 1992; Kellogg et al., 2003). Since nothing can
be done to exclude populations of obligate hyperparasitoids in nature, this predicament puts
pressure of biological control practitioners to investigate ways of stabilizing biological control
programmes in the light of ecological disturbance from obligate hyperparasitoids.
As a potential solution to this problem, I investigated the influence of differential vulnerability
of primary parasitoid species in a community to obligate hyperparasitoids in mitigating effects of
hyperparasitism on biological control using the P. xylostella natural system in South Africa as a
model. In this system, only immature stages of the most abundant primary parasitoid species (C.
vestalis) are vulnerable to resident obligate hyperparasitoid species (Waladde et al., 2001;
Mosiane et al., 2003; Smith, 2004; Nofemela and Kfir, 2008). This study showed that as
hyperparasitism levels increased, population density of C. vestalis declined significantly.
However, the impact of hyperparasitoids on C. vestalis populations did not negatively influence
total primary parasitism levels nor led to high P. xylostella infestations. This was a consequence
of significant increases in population densities of unaffected primary parasitoid species (i.e., O.
sokolowskii and D. collaris) that took advantage of the higher availability of unparasitized hosts
as populations of C. vestalis declined.
Since population densities of both O. sokolowskii and D. collaris were negatively related to
that of C. vestalis, it can be inferred that the higher efficiency of C. vestalis in utilizing young
host larvae (Nofemela, 2004) limited availability of suitable hosts for O. sokolowskii and D.
collaris at low hyperparasitism levels. It is widely observed that parasitoid species that attack
early host life stages have an advantage of access to abundant host resource over those attacking
advanced host life stages (Price, 1972; Chesson, 1991), except where the latter are able to utilize
parasitized hosts (Briggs, 1993; Oishi and Sato, 2008). Since some potential hosts are missed by
female parasitoids in the field (Godfray, 1994), the numerical dominance of the primary
parasitoid species attacking early host life stages does not preclude coexistence with parasitoid
species attacking advanced host life stages on the host population. As a consequence, changes in
the population density of the dominant species have knock-on effect on population density of
other species in the community such that as population density of the latter will increase when
population density of the former decline (Müller and Godfray, 1999). Although D. collaris
cannot utilize pupae already parasitized by other parasitoid species particularly larval-pupal
parasitoids like O. sokolowskii (Liu et al., 2001), and thus it is at the mercy of hosts missed by
parasitoids attacking P. xylostella larvae, of which the larval endoparasitoid C. vestalis is the
most dominant, O. sokolowskii can utilize some hosts containing C. ves-talis larvae.
With few exceptions (Alam, 1992; Cock, 1983; Nofemela and Kfir, 2008; this study), the
facultative hyperparasitic habit of O. sokolowskii is considered to have a negative effect on C.
vestalis population density, and thus on total primary parasitism of P. xylostella (Talekar and Hu,
1996). The ability of facultative hyperparasitoids to develop both as primary parasitoids and as
hyperparasitoids is thought to give them an advantage over susceptible primary parasitoids
(Rosenheim et al., 1995; Sullivan and Völkl, 1999; Pérez-Lachaud et al., 2004). However, this
advantage depends greatly on whether or not the facultative hyperparasitoid in question has
superior or at least comparable searching efficiency, fertility and intrinsic rate of population
increase compared to the primary parasitoid (Pedersen and Mills, 2004), in addition to ability to
utilize the immature stages of the intra-guild prey. Laboratory studies showed that C. vestalis is a
superior competitor to O. sokolowskii at intra-host level (Mahmood et al., 2003; Shi and Liu,
2003), as it uses physical combat of 1st instar larvae and physiological suppression, i.e., due to
polydnavirus and venom injected by the mother in the P. xylostella host during oviposition, to
overcome interspecific competition (Bai et al., 2011). But, as C. vestalis larvae grow in size and
get too close to the integument of the host, they may be vulnerable to direct parasitism by O.
sokolowskii (Mahmood et al., 2003; Shu-Sheng Liu, Zhejiang University, personal
communication). Thus, O. sokolowskii has a narrow window of opportunity to directly parasitize
C. vestalis due to the restriction imposed by its virtually invisible ovipositor. This explains why
direct exposure of P. xylostella larvae containing C. vestalis larvae to O. sokolowskii yields
lower proportion of secondary parasitism (Mahmood et al., 2003; Xue-Xin Chen, Zhejiang
University, personal communication). In this study, O. sokolowskii was significantly more of a
primary parasitoid than a hyperparasitoid, and its realized clutch size was significantly higher on
pupae of P. xylostella than of C. vestalis, which suggests that if O. sokolowskii cannot discriminate between unparasitized host larvae and host larvae parasitized by C. vestalis, and
adjusts its clutch size accordingly, parasitism of P. xylostella larvae containing C. vestalis larvae
carries a high cost for its population density. Further, its impact on C. ves-talis population
appeared random as it was not related to density of P. xylostella larvae. Thus, it is inconceivable
that O. sokolowskii actively searches for and parasitizes host larvae containing C. vestalis larvae
of vulnerable size, and avoid unparasitized hosts. At population level, the advantage of C.
vestalis over O. sokolowskii is due to faster generation time and higher fertility (Wang et al.,
1999; Shi et al., 2002; Shi and Liu, 2003).
The positive influence of natural enemy diversity on biological control of insect pests was
reported in several studies in recent years (Walde, 1994; Rosenheim, 1998; Wilson et al., 1999;
Rodríguez and Hawkins, 2000; Rozdisky and Stone, 2001; Cardinale et al., 2003; Casula et al.,
2006). However, to the best of my knowledge, the relationship between natural enemy diversity
and population suppression of insect pests was never studied in the context of ecological
disturbance from higher order consumers. This study showed that primary parasitoid species that
are invulnerable to hyperparasitism can take over the function of vulnerable ones in communities
with strong interspecific interactions. Therefore, a whole ecosystem approach that considers both
direct and indirect effects of hyperparasitoids in primary parasitoid communities will improve
our understanding of the net impact of hyperparasitism on biological control of insect pests.
Acknowledgments
I thank M.S. Mosiane, T.M. Mailula, M. Ngoato, P.H. Dikobe, M. Motsamai, and D. Pooe for
technical assistance. The helpful discussions with K.V. Mawela and Dr. D.O. Simelane during
preparation of this manuscript are highly appreciated. The study was financed by the Agricultural
Research Council, the Department of Science and Technology, and the United States Agency for
International Development (USAID) – CDR (Grant no. TA-MOV-C18-055).
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